Drosophilids with darker cuticle have higher body temperature under light

Abstract

Cuticle pigmentation was shown to be associated with body temperature for several relatively large species of insects, but it was questioned for small insects. Here we used a thermal camera to assess the association between drosophilid cuticle pigmentation and body temperature increase when individuals are exposed to light. We compared mutants of large effects within species (Drosophila melanogaster ebony and yellow mutants). Then we analyzed the impact of naturally occurring pigmentation variation within species complexes (Drosophila americana/Drosophila novamexicana and Drosophila yakuba/Drosophila santomea). Finally we analyzed lines of D. melanogaster with moderate differences in pigmentation. We found significant differences in temperatures for each of the four pairs we analyzed. The temperature differences appeared to be proportional to the differently pigmented area: between Drosophila melanogaster ebony and yellow mutants or between Drosophila americana and Drosophila novamexicana, for which the whole body is differently pigmented, the temperature difference was around 0.6 °C ± 0.2 °C. By contrast, between D. yakuba and D. santomea or between Drosophila melanogaster Dark and Pale lines, for which only the posterior abdomen is differentially pigmented, we detected a temperature difference of about 0.14 °C ± 0.10 °C. This strongly suggests that cuticle pigmentation has ecological implications in drosophilids regarding adaptation to environmental temperature.

Figure 1

Synthesis pathway of cuticle pigments in Drosophila melanogaster.

Figure 2

(a) Picture of ebony¹ (left) and yellow¹ (right) Drosophila melanogaster females. (b) Boxplots showing the normalized temperatures in °C for D. melanogaster ebony (E) and yellow (Y) mutant females. Pairs of individuals recorded simultaneously are indicated by lines. In all pairs, the ebony fly is hotter than the yellow fly. This is confirmed by a Wilcoxon rank signed test showing that E is significantly hotter than Y (p-value p = 0.00072, V = 120 being the value of the test statistic). ***p < 0.001.

Figure 3

(a) Picture of D. americana (left) and D. novamexicana (right). (b) Boxplots showing the normalized temperatures in °C for D. americana (A) and D. novamexicana (NM) females. Pairs of individuals recorded simultaneously are indicated by lines. In all pairs, the D. americana individual is hotter than the D. novamexicana individual. This is confirmed by a Wilcoxon rank signed test showing that A is significantly hotter than NM (p-value p = 0.00024, V = 91 being the value of the test statistic). ***p < 0.001.

Figure 4

(a) Picture of Drosophila yakuba (left) and Drosophila santomea (right) males. (b) Boxplots showing the normalized temperatures in °C for D. yakuba (Y) and D. santomea (S) males. Pairs of individuals recorded simultaneously are indicated by lines. In all pairs but one, the D. yakuba individual is hotter than the D. santomea individual. This is confirmed by a Wilcoxon rank signed test showing that Y is significantly hotter than S (p-value p = 0.0012, V = 3 being the value of the test statistic). **p < 0.01.

Figure 5

(a) Picture of Drosophila melanogaster Dark (left) and Pale (right) females. (b) Boxplots showing the normalized temperatures in °C for D. melanogaster Dark (D) and Pale (P) females. Pairs of individuals recorded simultaneously are indicated by lines. In all pairs but one, the Dark individual is hotter than the Pale individual. This is confirmed by a Wilcoxon rank signed test showing that D is significantly hotter than P (p-value p = 0.00049, with V = 90 being the value of the test statistic). ***p < 0.001.

Figure 6

Graph showing the relation between pigmentation differences and temperature differences for the four pairs of comparisons (means and standard deviations). Pigmentation and temperature were not measured on the same individuals.

Figure 7

Evolution of fly body temperatures in an experiment with D. melanogaster ebony and yellow mutants. (a) snapshot taken after the light was switched on (lowest temperature is blue, hottest temperature is white). (b) temperature curves of the two flies recorded during the whole course of the experiment.

Figure 8

Principle of temperature normalization. In this screenshot of a video taken with the FLIR camera, Drosophila santomea is on the left and Drosophila yakuba is on the right. The flies are surrounded by eight ellipses numbered 1 to 8. The regions denoted by “Freehand” delimit the areas covered by the bodies of the two flies monitored during the experiment. In this example, ellipses 4 to 7 were used to normalize the body temperature of the fly to the left, while ellipses 1, 2, 3 and 8 were used to normalize the body temperature of the fly to the right.